Emma J. Sayer

Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems

The widespread use of forest litter as animal bedding in central Europe for many centuries gave rise to the first litter manipulation studies, and their results demonstrated that litter and its decomposition are a vital part of ecosystem function. Litter plays two major roles in forest ecosystems: firstly, litterfall is an inherent part of nutrient and carbon cycling, and secondly, litter forms a protective layer on the soil surface that also regulates microclimatic conditions. By reviewing 152 years of litter manipulation experiments, I show that the effects of manipulating litter stem from changes in one, or both, of these two functions, and interactions between the variables influenced by the accumulation of litter can result in feedback mechanisms that may intensify treatment effects or mask responses, making the interpretation of results difficult.

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest

We maintained a factorial nitrogen (N), phosphorus (P), and potassium (K) addition experiment for 11 years in a humid lowland forest growing on a relatively fertile soil in Panama to evaluate potential nutrient limitation of tree growth rates, fine-litter production, and fine-root biomass. We replicated the eight factorial treatments four times using 32 plots of 40 x 40 m each. The addition of K was associated with significant decreases in stand-level fine-root biomass and, in a companion study of seedlings, decreases in allocation to roots and increases in height growth rates. The addition of K and N together was associated with significant increases in growth rates of saplings and poles (1-10 cm in diameter at breast height) and a further marginally significant decrease in stand-level fine-root biomass. The addition of P was associated with a marginally significant (P = 0.058) increase in fine-litter production that was consistent across all litter fractions. Our experiment provides evidence that N, P, and K all limit forest plants growing on a relatively fertile soil in the lowland tropics, with the strongest evidence for limitation by K among seedlings, saplings, and poles.

Increased litterfall in tropical forests boosts the transfer of soil CO2 to the atmosphere.

Aboveground litter production in forests is likely to increase as a consequence of elevated atmospheric carbon dioxide (CO2) concentrations, rising temperatures, and shifting rainfall patterns. As litterfall represents a major flux of carbon from vegetation to soil, changes in litter inputs are likely to have wide-reaching consequences for soil carbon dynamics. Such disturbances to the carbon balance may be particularly important in the tropics because tropical forests store almost 30% of the global soil carbon, making them a critical component of the global carbon cycle; nevertheless, the effects of increasing aboveground litter production on belowground carbon dynamics are poorly understood. We used long-term, large-scale monthly litter removal and addition treatments in a lowland tropical forest to assess the consequences of increased litterfall on belowground CO2 production. Over the second to the fifth year of treatments, litter addition increased soil respiration more than litter removal decreased it; soil respiration was on average 20% lower in the litter removal and 43% higher in the litter addition treatment compared to the controls but litter addition did not change microbial biomass. We predicted a 9% increase in soil respiration in the litter addition plots, based on the 20% decrease in the litter removal plots and an 11% reduction due to lower fine root biomass in the litter addition plots. The 43% measured increase in soil respiration was therefore 34% higher than predicted and it is possible that this ‘extra’ CO2 was a result of priming effects, i.e. stimulation of the decomposition of older soil organic matter by the addition of fresh organic matter. Our results show that increases in aboveground litter production as a result of global change have the potential to cause considerable losses of soil carbon to the atmosphere in tropical forests.

Increased Litterfall Changes Fine Root Distribution in a Moist Tropical Forest

Root proliferation into the Oa and Oe soil horizons in tropical forests is often substantial and allows direct cycling of nutrients from the organic matter; this was thought to be an adaptation to the low nutrient supply in infertile soils. In this study, we show that experimentally increased litter inputs promote root proliferation into the Oi and Oe horizons in a relatively fertile soil, suggesting that it is a response to a more readily available nutrient source rather than an adaptation to nutrient shortage, and the absence of root mats on fertile tropical soils is simply a consequence of the lack of persistent organic horizons due to high decomposition rates.

Leaf-cutting ants as ecosystem engineers: topsoil and litter perturbations around Atta cephalotes nests reduce nutrient availability

Despite considerable research into the effects of leaf‐cutting ant nests, the potential occurrence of low‐nutrient soils at nest sites has hitherto gone undetected. Leaf litter cover and topsoil conditions (organic carbon, total nitrogen, soil acidity, cation exchange capacity) were assessed along transects running from nests of eight adult Atta cephalotes colonies into the understorey of Atlantic forest to examine the extent of nest effects. Nests were virtually free of leaf litter (c. 150 g m−2) and litter cover increased along a saturating curve with nest distance, reaching 1300 g m−2 in the undisturbed forest. Soil acidity and nutrient concentrations were strongly correlated with leaf litter cover (r = 0.66–0.72) for both soil types occurring in the study region. Total soil nitrogen concentration varied from 0.2 g kg−1 in sandy nest soil and 0.5 g kg−1 in clay‐rich nest soil to 0.5 and 1.3 g kg−1, respectively, at a distance of 24 m from nests, while soil carbon concentration ranged from 2.1 to 6.1 g kg−1 (sandy soil) and 4.5 to 15.7 g kg−1 (clay‐rich soil) over the same distance. Nest‐associated variations in edaphic parameters suggest that each colony affected an area of up to 0.5 ha. In contrast to the common perception that leaf‐cutting ant activities increase nutrient availability, our results suggest that their territories are characterised by reduced levels of leaf litter and, consequently, soil nutrients. The observed nutrient depletion must be taken into account when considering the potential impacts of ant nests for plant regeneration.

The role of tree size in the leafing phenology of a seasonally dry tropical forest in Belize, Central America

Leafing phenology of two dry-forest sites on soils of different depth (S = shallow, D = deep) at Shipstern Reserve, Belize, were compared at the start of the rainy season (April-June 2000). Trees 2.5 cm dbh were recorded weekly for 8 wk in three 0.04-ha plots per site. Ten species were analysed individually for their phenological patterns, of which the three most common were Bursera simaruba, Metopium brownei and Jatropha gaumeri. Trees were divided into those in the canopy (> 10 cm dbh) and the subcanopy ( 10 cm dbh). Site S had larger trees on average than site D. The proportion of trees flushing leaves at any one time was generally higher in site S than in site D, for both canopy and subcanopy trees. Leaf flush started 2 wk earlier in site S than site Dfor subcanopy trees, but only 0.5 wk earlier for the canopy trees. Leaf flush duration was 1.5 wk longer in site S than site D. Large trees in the subcanopy flushed leaves earlier than small ones at both sites but in the canopy just at site D. Large trees flushed leaves earlier than small ones in three species and small trees flushed leaves more rapidly in two species. Bursera and Jatropha followed the general trends but Metopium, with larger trees in site Dthan site S, showed the converse with onset of flushing 1 wk earlier in site Dthan site S. D ifferences in response of the canopy and subcanopy trees on each site can be accounted for by the predominance of spring-flushing or stem-succulent species in site S and a tendency for evergreen species to occur in site D. Early flushing of relatively larger trees in site D most likely requires access to deeper soil water reserves but small and large trees utilize stored tree water in site S.

Arbuscular mycorrhizal fungal community composition is altered by long-term litter removal but not litter addition in a lowland tropical forest

Tropical forest productivity is sustained by the cycling of nutrients through decomposing organic matter. Arbuscular mycorrhizal (AM) fungi play a key role in the nutrition of tropical trees, yet there has been little experimental investigation into the role of AM fungi in nutrient cycling via decomposing organic material in tropical forests. We evaluated the responses of AM fungi in a long-term leaf litter addition and removal experiment in a tropical forest in Panama. We described AM fungal communities using 454-pyrosequencing, quantified the proportion of root length colonised by AM fungi using microscopy, and estimated AM fungal biomass using a lipid biomarker. AM fungal community composition was altered by litter removal but not litter addition. Root colonisation was substantially greater in the superficial organic layer compared with the mineral soil. Overall colonisation was lower in the litter removal treatment, which lacked an organic layer. There was no effect of litter manipulation on the concentration of the AM fungal lipid biomarker in the mineral soil. We hypothesise that reductions in organic matter brought about by litter removal may lead to AM fungi obtaining nutrients from recalcitrant organic or mineral sources in the soil, besides increasing fungal competition for progressively limited resources.

Links between soil microbial communities and plant traits in a species-rich grassland under long-term climate change

Abstract Climate change can influence soil microorganisms directly by altering their growth and activity but also indirectly via effects on the vegetation, which modifies the availability of resources. Direct impacts of climate change on soil microorganisms can occur rapidly, whereas indirect effects mediated by shifts in plant community composition are not immediately apparent and likely to increase over time. We used molecular fingerprinting of bacterial and fungal communities in the soil to investigate the effects of 17 years of temperature and rainfall manipulations in a species‐rich grassland near Buxton, UK. We compared shifts in microbial community structure to changes in plant species composition and key plant traits across 78 microsites within plots subjected to winter heating, rainfall supplementation, or summer drought. We observed marked shifts in soil fungal and bacterial community structure in response to chronic summer drought. Importantly, although dominant microbial taxa were largely unaffected by drought, there were substantial changes in the abundances of subordinate fungal and bacterial taxa. In contrast to short‐term studies that report high resistance of soil fungi to drought, we observed substantial losses of fungal taxa in the summer drought treatments. There was moderate concordance between soil microbial communities and plant species composition within microsites. Vector fitting of community‐weighted mean plant traits to ordinations of soil bacterial and fungal communities showed that shifts in soil microbial community structure were related to plant traits representing the quality of resources available to soil microorganisms: the construction cost of leaf material, foliar carbon‐to‐nitrogen ratios, and leaf dry matter content. Thus, our study provides evidence that climate change could affect soil microbial communities indirectly via changes in plant inputs and highlights the importance of considering long‐term climate change effects, especially in nutrient‐poor systems with slow‐growing vegetation.

The Automated Root Exudate System (ARES) : a method to apply solutes at regular intervals to soils in the field

Summary Root exudation is a key component of nutrient and carbon dynamics in terrestrial ecosystems. Exudation rates vary widely by plant species and environmental conditions, but our understanding of how root exudates affect soil functioning is incomplete, in part because there are few viable methods to manipulate root exudates in situ. To address this, we devised the Automated Root Exudate System (ARES), which simulates increased root exudation by applying small amounts of labile solutes at regular intervals in the field. The ARES is a gravity‐fed drip irrigation system comprising a reservoir bottle connected via a timer to a micro‐hose irrigation grid covering c. 1 m2; 24 drip‐tips are inserted into the soil to 4‐cm depth to apply solutions into the rooting zone. We installed two ARES subplots within existing litter removal and control plots in a temperate deciduous woodland. We applied either an artificial root exudate solution (RE) or a procedural control solution (CP) to each subplot for 1 min day−1 during two growing seasons. To investigate the influence of root exudation on soil carbon dynamics, we measured soil respiration monthly and soil microbial biomass at the end of each growing season. The ARES applied the solutions at a rate of c. 2 L m−2 week−1 without significantly increasing soil water content. The application of RE solution had a clear effect on soil carbon dynamics, but the response varied by litter treatment. Across two growing seasons, soil respiration was 25% higher in RE compared to CP subplots in the litter removal treatment, but not in the control plots. By contrast, we observed a significant increase in microbial biomass carbon (33%) and nitrogen (26%) in RE subplots in the control litter treatment. The ARES is an effective, low‐cost method to apply experimental solutions directly into the rooting zone in the field. The installation of the systems entails minimal disturbance to the soil and little maintenance is required. Although we used ARES to apply root exudate solution, the method can be used to apply many other treatments involving solute inputs at regular intervals in a wide range of ecosystems.

Dung beetle community dynamics in undisturbed tropical forests:implications for ecological evaluations of land-use change

The impacts of human activities on tropical forests are widespread and increasing. Hence, a good knowledge base about ecological processes in undisturbed tropical forest is crucial to provide a baseline for evaluating anthropogenic change. Our 5‐year study focused on understanding the background spatial and inter‐annual variation in dung beetle communities at 12 sites of undisturbed lowland tropical rainforest in the Brazilian Amazon. We then assessed how this variation may affect ecological evaluations of anthropogenic influence by comparing community metrics with comparable dung beetle data collected from 15 sites of Eucalyptus plantation in the same region. Of all measured environmental variables, soil texture best explained spatial variation in dung beetle communities in undisturbed forests. Furthermore, soil texture was important for community assembly as it was associated with dung beetle nesting behaviours. While the relative abundance of dung beetle functional groups was stable over time, there were important inter‐annual temporal dynamics, with a fivefold variation in abundance and body mass, and with species richness ranging from 52 to 74. These temporal oscillations were probably caused by variation in dry season rainfall. This inter‐annual variation influenced the comparison between undisturbed forests and plantations, which could lead to inconsistencies in evaluation of anthropogenic change. We therefore highlight the importance of understanding natural variation in studies evaluating the consequences of land‐use change and other forest disturbances on forest biodiversity.